Abstract
Marine dinoflagellates produce a diversity of polyketide toxins that are accumulated in marine food webs and are responsible for a variety of seafood poisonings. Reef-associated dinoflagellates of the genus Gambierdiscus produce toxins responsible for ciguatera poisoning (CP), which causes over 50,000 cases of illness annually worldwide. The biosynthetic machinery for dinoflagellate polyketides remains poorly understood. Recent transcriptomic and genomic sequencing projects have revealed the presence of Type I modular polyketide synthases in dinoflagellates, as well as a plethora of single domain transcripts with Type I sequence homology. The current transcriptome analysis compares polyketide synthase (PKS) gene transcripts expressed in two species of Gambierdiscus from French Polynesia: a highly toxic ciguatoxin producer, G. polynesiensis, versus a non-ciguatoxic species G. pacificus, each assembled from approximately 180 million Illumina 125 nt reads using Trinity, and compares their PKS content with previously published data from other Gambierdiscus species and more distantly related dinoflagellates. Both modular and single-domain PKS transcripts were present. Single domain β-ketoacyl synthase (KS) transcripts were highly amplified in both species (98 in G. polynesiensis, 99 in G. pacificus), with smaller numbers of standalone acyl transferase (AT), ketoacyl reductase (KR), dehydratase (DH), enoyl reductase (ER), and thioesterase (TE) domains. G. polynesiensis expressed both a larger number of multidomain PKSs, and larger numbers of modules per transcript, than the non-ciguatoxic G. pacificus. The largest PKS transcript in G. polynesiensis encoded a 10,516 aa, 7 module protein, predicted to synthesize part of the polyether backbone. Transcripts and gene models representing portions of this PKS are present in other species, suggesting that its function may be performed in those species by multiple interacting proteins. This study contributes to the building consensus that dinoflagellates utilize a combination of Type I modular and single domain PKS proteins, in an as yet undefined manner, to synthesize polyketides.
Highlights
Benthic dinoflagellates of the genus Gambierdiscus are the primary source of ciguatoxins, neurotoxins responsible for ciguatera poisoning (CP), the most prevalent seafood toxin-associated illness in the world [1, 2]
The identification of polyketide synthase (PKS) genes in dinoflagellates has been hampered by their enormous genome sizes to obtain genome sequences, with the exception of Symbiodinium spp. [31, 69, 70, 71] and the parasite Amoebophyya ceratii [72], which have comparatively compact genome sizes
Most studies to date have been limited to transcriptome analysis, which has yielded a consensus that dinoflagellates possess both Type I modular and standalone PKS domains that may function in concert with modular PKSs by providing activity in trans, and/ or may form separate Type II -like complexes [73, 74]
Summary
Benthic dinoflagellates of the genus Gambierdiscus are the primary source of ciguatoxins, neurotoxins responsible for ciguatera poisoning (CP), the most prevalent seafood toxin-associated illness in the world [1, 2]. Ciguatoxins bind to voltage-gated sodium channels, present in brain, skeletal muscle, heart, peripheral nervous system, and sensory neurons, causing voltage independent activation and prolonged opening of the channels, which results in spontaneous and repetitive action potentials that alter sensorimotor conduction [1]. In humans, their consumption results in CP, with acute symptoms that may include diarrhea, vomiting, muscular and joint aches, numbness and tingling of the mouth and extremities, cold allodynia, irregular heartbeat, and rarely, respiratory paralysis [1,2]. 20 percent of CP cases progress to chronic ciguatera, with debilitating symptoms similar to chronic fatigue syndrome that may last from months to years [3]
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